Abstract
Hybridization between species is an important mechanism for the origin of novel lineages and adaptation to new environments. Increased allelic variation and modification of the transcriptional network are the two recognized forces currently deemed to be responsible for the phenotypic properties seen in hybrids. However, since the majority of the biological functions in a cell are carried out by protein complexes, inter-specific protein assemblies therefore represent another important source of natural variation upon which evolutionary forces can act. Here we studied the composition of six protein complexes in two different Saccharomyces “sensu stricto” hybrids, to understand whether chimeric interactions can be freely formed in the cell in spite of species-specific co-evolutionary forces, and whether the different types of complexes cause a change in hybrid fitness. The protein assemblies were isolated from the hybrids via affinity chromatography and identified via mass spectrometry. We found evidence of spontaneous chimericity for four of the six protein assemblies tested and we showed that different types of complexes can cause a variety of phenotypes in selected environments. In the case of TRP2/TRP3 complex, the effect of such chimeric formation resulted in the fitness advantage of the hybrid in an environment lacking tryptophan, while only one type of parental combination of the MBF complex allowed the hybrid to grow under respiratory conditions. These phenotypes were dependent on both genetic and environmental backgrounds. This study provides empirical evidence that chimeric protein complexes can freely assemble in cells and reveals a new mechanism to generate phenotypic novelty and plasticity in hybrids to complement the genomic innovation resulting from gene duplication. The ability to exchange orthologous members has also important implications for the adaptation and subsequent genome evolution of the hybrids in terms of pattern of gene loss.
Highlights
The Saccharomyces sensu stricto yeasts represent a diverse, monophyletic group of species that have the ability to produce viable and stable hybrids that can propagate mitotically
When comparing the growth of the four strains bearing different combinations of TRP2/TRP3 protein complexes, we found that the strain with the Trp2pSu/Trp3pSc chimeric complex grew much better than all the other strains in a medium lacking tryptophan (Figure 3B)
In the case of MBF complex, we have shown an example of phenotypic plasticity of different chimeric assemblies, and found a novel case of hybrid incompatibility between S. cerevisiae and S. uvarum when cells are grown on a non–fermentable medium and the mitochondria function become essential for cell viability
Summary
The Saccharomyces sensu stricto yeasts represent a diverse, monophyletic group of species that have the ability to produce viable and stable hybrids that can propagate mitotically. In the hybrid cellular environment, where two sets of homologous proteomes coexist, there is the potential for the cell to form chimeric assemblies between homologus protein complexes. Spontaneous chimeric assemblies may widen the adaptation potential of the cell, since several different combinations of the same protein complex can be used. Such situation can lead to new phenotypic variants that are beneficial to the hybrid in novel contexts. Chimericity in protein-protein interaction represents a potentially important mechanism for generating phenotypic diversity upon which evolutionary forces can act, and may constitute a molecular explanation of hybrid vigour
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